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Domoic Acid Contamination Within Eight Representative Species from the Benthic Food Web of Monterey Bay, California, USA

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Domoic Acid Contamination Within Eight Representative Species from the Benthic Food Web of Monterey Bay, California, USA Vol. 367: 35–47, 2008 MARINE ECOLOGY PROGRESS SERIES Published September 11 doi: 10.3354/meps07569 Mar Ecol Prog Ser Domoic acid contamination within eight representative species from the benthic food web of Monterey Bay, California, USA Rikk G. Kvitek1,*, Judah D. Goldberg2, G. Jason Smith3, Gregory J. Doucette4, Mary W. Silver5 1Division of Science and Environmental Policy, California State University Monterey Bay, 100 Campus Center, Seaside, California 93955, USA 2NortekUSA, 2709 51st Avenue SW, Seattle, Washington 98116, USA 3Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, California 95039, USA 4Marine Biotoxins Program, NOAA/National Ocean Service, 219 Fort Johnson Road, Charleston, South Carolina 29412, USA 5Department of Ocean Sciences, University of California at Santa Cruz, 1156 High Street, Santa Cruz, California 95064, USA ABSTRACT: Benthic food webs often derive a significant fraction of their nutrient inputs from phyto- plankton in the overlying waters. If the phytoplankton include harmful algal species like Pseudo- nitzschia australis, a diatom capable of producing the neurotoxin domoic acid (DA), the benthic food web can become a depository for phycotoxins. We tested the general hypothesis that DA contami- nates benthic organisms during local blooms of P. australis, a widespread toxin producer along the US west coast. To test for trophic transfer and uptake of DA into the benthic food web, we sampled 8 benthic species comprising 4 feeding groups: filter feeders (Emerita analoga and Urechis caupo); a predator (Citharichthys sordidus); scavengers (Nassarius fossatus and Pagurus samuelis) and deposit feeders (Neotrypaea californiensis, Dendraster excentricus and Olivella biplicata). Sampling occurred before, during and after blooms of P. australis in Monterey Bay, CA, USA during 2000 and 2001. DA was detected in all 8 species, with contamination persisting over variable time scales. Max- imum DA levels in N. fossatus (674 ppm), E. analoga (278 ppm), C. sordidus (515 ppm), N. californien- sis (145 ppm), P. samuelis (56 ppm), D. excentricus (15 ppm) and O. biplicata (3 ppm) coincided with P. australis blooms, while DA levels in U. caupo remained above 200 ppm (max. = 751 ppm) through- out the study period. DA in 6 species exceeded levels thought to be safe for higher level consumers (i.e. ≥20 ppm) and thus is likely to have deleterious effects on marine birds, sea lions and the endan- gered California sea otter, known to prey upon these benthic species. KEY WORDS: Domoic acid · Food web · Benthic · Harmful algal bloom · Pseudo-nitzschia · Trophic transfer Resale or republication not permitted without written consent of the publisher INTRODUCTION to marine predators. Harmful algal species are found worldwide (Smayda 1989, 1992, Hallegraeff 1993), and Phytoplankton are the base of marine food webs, their adverse effects have been manifested in numer- supporting filter feeders, micro-grazers and ultimately ous mass mortalities of fish, birds and marine mammals most marine animals via trophic transfer of the organic (Work et al. 1993, Lefebvre et al. 1999, Scholin et al. matter they produce photosynthetically. Certain spe- 2000, Shumway et al. 2003, Landsberg et al. 2005). cies of phytoplankton, however, produce compounds The water soluble phycotoxin domoic acid (DA) is a toxic to other organisms. When these harmful algal spe- rigid analog of the excitatory amino acid glutamate cies proliferate, the same trophic transfer processes that that binds to glutamate receptors causing neuro- build food webs provide for transfer of potent biotoxins excitation or cell degeneration in vertebrate brains *Email: [email protected] © Inter-Research 2008 · www.int-res.com 36 Mar Ecol Prog Ser 367: 35–47, 2008 and, in sufficient concentrations, causes disorientation, Altwein et al. 1995, Douglas et al. 1997) since the 1987 memory loss, seizures, coma and death. The resulting ASP event in Canada, when 3 people died after con- intoxication syndrome is known as DA poisoning suming contaminated blue mussels Mytilus edulis (DAP) (Lund et al. 1997) or amnesic shellfish poisoning (Quilliam & Wright 1989), but little is known regard- (ASP) in cases of human exposure related to shellfish ing the uptake and retention of DA in other benthic consumption (Perl et al. 1990). DA can be produced by organisms. some species of diatoms, including several from the The purpose of the present study was to test the gen- genus Pseudo-nitzschia (Fritz et al. 1992, Garrison et eral hypothesis that DA derived from overlying waters al. 1992). Bivalve filter feeders grazing upon dense is transferred into benthic food webs in a nearshore blooms of DA-producing Pseudo-nitzschia were the environment. Our approach was to monitor the water earliest described vectors, passing the toxin on to column for DA-producing Pseudo-nitzschia, toxin con- human consumers (Quilliam & Wright 1989, Wright et centration and benthic species representing 4 different al. 1989). Subsequently, Northern anchovies Engraulis feeding modes for the uptake and retention of DA over mordax have been described as vectors of DA to sea a 2 yr period in Monterey Bay, CA. These results were lions (Lefebvre et al. 1999, Scholin et al. 2000) and used to evaluate the following 6 specific hypotheses: marine birds (Fritz et al. 1992); and krill (euphausiids) H1: Pseudo-nitzschia cell density can serve as a reli- appear to be the carrier of DA to squid and baleen able proxy in the present study for DA toxin concen- whales (Bargu et al. 2002, Lefebvre et al. 2002). tration in the water column. Anchovy and krill are now recognized as key pelagic H2: Surface water DA concentration can serve as a vector species of DA because of their abundance and reliable proxy in the present study for DA concentra- central position in the pelagic food chain: both species tions near the seafloor and in contact with the benthos are conspicuous planktivores that offer immediate (i.e. whether or not the benthos is exposed to elevated trophic links from primary producers to higher trophic- DA concentrations during bloom periods detected at level consumers such as birds, pinnipeds and even the surface). cetaceans. H3: Benthic species accumulate measurable In Monterey Bay, California, USA, an area subject to amounts of DA during bloom events in proportion to recurring blooms of toxic Pseudo-nitzschia (Bates et al. DA concentration in the water column. 1989, Fritz et al. 1992, Garrison et al. 1992, Scholin et H4: DA body burdens in benthic species are signifi- al. 2000), DAP events have been well documented and cantly lower during non-bloom periods when DA is not the toxin shown to be incorporated into pelagic food detectable in the water column. webs, but trophic transfer of DA into the benthic food H5: DA body burdens in benthic species remain ele- web is poorly understood, except for those benthic spe- vated during non-bloom periods when DA is not cies used or proposed for monitoring purposes (i.e. detectable in the water column. mussels, Langlois et al. 1993; and sand crabs, Ferdin et H6: Patterns in DA uptake and retention in the ben- al. 2002). Predators and scavengers feeding upon con- thic food web vary with trophic level. taminated organisms at depth could be exposed to DA To study the uptake and retention of DA in the ben- produced in overlying waters (i.e. Lund et al. 1997). thic food web, we collected 8 benthic species including Also, in shallow neritic environments, where the the filter-feeding echiuran worm Urechis caupo, the euphotic zone can extend to the bottom, blooms of common filter-feeding sand crab Emerita analoga, the Pseudo-nitzschia may encompass the entire water col- scavenging snail Nassarius fossatus, the predatory flat umn and be in contact with the seafloor. As a result, fish Citharichthys sordidus, the deposit-feeding ghost benthic organisms and other mid-water species may shrimp Neotrypaea californiensis, the scavenging be directly exposed to high concentrations of parti- hermit crab Pagurus samuelis, the deposit- and filter- culate DA. Additionally, as Pseudo-nitzschia cell den- feeding sand dollar Dendraster excentricus and the sities rise, flocculation of the chains can occur (De deposit-feeding olive snail Olivella biplicata (Ricketts Philippis et al. 2005), with subsequent sinking of the et al. 1985). Collections occurred during 2000 and aggregates and resultant delivery of toxic food bundles 2001, 2 years in which DA-producing Pseudo-nitzschia to bottom dwellers. The benthic environment may then blooms were detected within Monterey Bay. become a source for DA contamination well after an These 8 organisms represent not only links within overlying Pseudo-nitzschia bloom subsides. Cells the benthic food chain, but serve as important connec- deposited onto the bottom may be ingested by benthic tions to higher trophic levels as well. Shore birds and deposit feeders or resuspended into the water column surf fish are known to feed upon Emerita analoga, and via bioturbation and bottom flow. DA has been the endangered California sea otter Enhydra lutris is a detected in a few commercially important bivalve and voracious predator of nearly all the organisms sampled crustacean shellfish species (Martin et al. 1993, in the present study (Wenner et al. 1987, Kvitek & Kvitek et al.: Domoic acid in Monterey Bay benthic food web 37 Oliver 1988, Blokpoel et al. 1989, Riedman & Estes an underwater scooter (Dacor SeaSprint) and excavat- 1990, Webber & Cech 1998). Herein we report Pseudo- ing the sandy bottom with bursts from the exhaust fan. nitzschia bloom-associated DA accumulation in di- The flat fish Citharichthys sordidus was collected by verse components of the Monterey Bay benthic com- spiking the fish through the operculum with a screw munity and discuss implications of this ‘pelagic to fastened at a right angle to the end of a 0.3 m PVC benthic to pelagic’ coupling for transfer of this potent pipe. Care was taken not to puncture the viscera of the neurotoxin to higher level consumers in this regional fish, which are the tissues analyzed for DA.
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